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Use of Soybean Meal in the Diets of Omnivorous Freshwater

By Delbert M. Gatlin III, Department of Wildlife and Sciences and Faculty of Nutrition, Texas A&M University System

Written in cooperation with the United Soybean Board and American Soybean Association

Abstract

World production is dominated by omnivorous fish species that live in freshwater, including various and species. Soybean meal is a prominent ingredient used in prepared diets for these species, often constituting 50 to 60% of the total formulation. Such levels of incorporation are possible due to adequate palatability of soybean meal and its excellent nutritional value for these species, including high levels of crude protein, complementary amino acid profile and relatively high nutrient digestibility. For many omnivorous freshwater species cultured throughout the world, soybean meal has largely replaced more costly protein feedstuffs in diet formulations, such as , while maintaining optimal fish production. As a result, the cost of fish production has been reduced substantially. While aquacultural production continues to expand worldwide to meet the growing demand for , the use of soybean products will play an even more important role in providing high-quality protein for various fish species.

Introduction (Anonymous, 2002). Various other Chinese carp species, such as the silver carp (Hypopthalmichthys Feedstuffs derived from soybean have been used molitrix), grass carp (Ctenopharyngodon idella), predominantly for many years in diet formulations bighead carp (Aristichthys nobilis), crucian carp for the aquacultural production of numerous fish (Carassius auratus gibelio) and mud carp (Cirrhinus species. As a group, various species mulitorella), are produced primarily in China, that exhibit omnivorous feeding behavior although more limited production occurs in other historically have been fed prepared diets containing parts of Asia and Europe (Stickney, 2000a). relatively high levels of soybean meal (up to 60% by weight). This group of fish constitutes the largest The Indian , such as the rohu (Labeo rohita), sector of world aquaculture production by tonnage mrigal (Cirrhinus mrigala) and catla (Catla catla), (Anonymous, 2002), and are a major user of are another group of carp species native to the Indian soybean products. subcontinent and produced predominantly there. These fish are produced primarily in fertilized ponds Fish Species with the use of supplemental feeds (Stickney, 2000a). Prominent members of this group of freshwater, omnivorous species include various cyprinids, such Catfish of the genus Ictalurus and Clarius also are as the (Cyprinus carpio), which has prominent freshwater, omnivorous species that are the historical distinction of being the first fish cultured in various parts of the world. The channel cultured during the fifth century B.C. in China catfish (Ictalurus punctatus) constitutes the largest (Stickney, 2000a). Aquacultural production of this aquacultural enterprise in North America, and also is species has been established in various countries in produced in Latin America and Asia (Tucker, 2000). Asia, Europe, Africa and Latin America for many Catfish of the genus Clarius, also known as the years and constitutes the largest sector of world “walking catfish,” are distributed throughout aquaculture in terms of quantity produced , Africa and the Near East, and are

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 1 cultured in some European countries (Stickney, Oil extraction of soybeans by the expeller process 2000b). The prominent species cultured in Asia results in a meal containing approximately 42% include Clarius batrachus and C. macrocephalus; protein (Li et al., 2000a). The amino acid whereas, the sharptooth catfish (Clarius gariepinus) composition of these soybean meals is similar when has been cultured in Africa and Europe. These expressed as a percent of protein, and represents the species have been cultured at various levels of most balanced profile of all plant proteins. Soybean intensity in earthen ponds and recirculating water meal without hulls has a reduced fiber content systems. The level of production intensity largely (approximately 3.4%) compared to the meal dictates the nutritional regime employed, which containing hulls (approximately 6.2%). Both of ranges from organic fertilization to nutritionally these meals have lipid content around 1% due to the complete prepared diets. efficient solvent extraction process. These two soybean meals have been used most frequently in Another group of warmwater, omnivorous species aquafeeds and therefore will receive most of the cultured throughout the world and comprising a consideration in this review. large portion of global production is various species (Oreochromis and Tilapia sp.) (Stickney, Another soybean product commonly referred to as 2000c). These fish are native to Africa and the full- soybean meal (FFSBM) is produced by heat Middle East, but have been cultured in tropical and treating whole soybeans. This product has a crude temperate regions around the world. They are protein content of approximately 38% (as-fed basis) produced at various levels of intensity in a wide and a lipid level of approximately 18%, providing range of culture systems, and nutritional regimes are high levels of linoleic and linolenic acids (Lim and adjusted accordingly. Akiyama, 1992). FFSBM has been evaluated and incorporated into diets of warmwater, omnivorous There are several other freshwater, omnivorous species to a more limited extent than coldwater species whose aquacultural production is currently carnivorous species, primarily due to the more limited to specific regions of the world. One such restrictive lipid levels typically included in the diets example is the silver (Bidyanus bidyanus), a of the former species. Adequate heat treatment of fish native to Australia that has demonstrated FFSBM is required to inactivate the heat-labile anti- excellent characteristics for aquacultural production nutritional factors known to be present in raw in earthen ponds. soybeans. Several different methods of heat treatment, including boiling and dry extrusion of the Soybean Products whole soybeans, have been employed.

Several different products derived from soybeans The nutritional value of properly heated FFSBM for have been evaluated using various fish species. various warmwater species is somewhat variable, These products all contain rather high levels of based on the limited number of published studies. In crude protein, ranging from 38 to 49% by weight. mirror carp (Cyprinus carpio), the value of FFSBM Soybean products are recognized for having the was reported to be equivalent of commercial most balanced amino acid composition of all plant soybean meal or soy protein concentrate feedstuffs, and the relative amounts of indispensable reconstituted with soybean oil (Viola et al., 1983). amino acids in these various products are very In contrast, Abel et al. (1984) reported that a diet similar when expressed as a percentage of crude containing 50% heat-treated FFSBM in place of half protein (Lim and Akiyama, 1992). The sulfur- the fish meal in a control diet supported growth of containing amino acids and cystine are mirror carp at only 60 to 65% of the control diet. generally considered to be most limiting in soybean This was attributed to an inferior amino acid balance products compared to the quantitative amino acid in the test diet, and supplementation of lysine, requirements of most fish species (NRC, 1993). methionine and threonine to the FFSBM diet, which enhanced the growth response of mirror carp. The most widely used soybean products in aquaculture diets are the meals resulting from the Hybrid tilapia (Oreochromis niloticus x O. aureus) removal of oil from the soybean. Solvent-extraction fed a diet in which 30% of the fish meal in the of the oil results in products that typically contain control diet was replaced with FFSBM had similar 44% crude protein if the soybean hulls are included weight gain, feed efficiency, protein efficiency ratio or 48% crude protein without the hulls (NRC, 1993).

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 2 and protein digestibility, compared to fish fed the protein concentrate. This product appears to be a control diet (Shiau et al., 1990). In another study, highly nutritious protein feedstuff based on the Nile tilapia (Oreochromis niloticus) fed boiled limited evaluations conducted to date, but its cost FFSBM as 58.3% of diet had similar weight gain, generally makes it prohibitive to use in most diet feed efficiency, apparent protein digestibility and formulations for fish. Possible exceptions might be apparent net protein utilization as fish fed a diet with its inclusion in diets designed for specific, time- 52.4% solvent-extracted soybean meal (Wee and restricted life stages such as the larval stages of some Shu, 1989). fish species (Escaffre et al., 1997).

Channel catfish also were reported to use FFSBM, Digestibility as well as commercial soybean meal (Saad, 1979). In that pond trial, catfish fed diets containing 37.2 and The digestibility or availability of various nutrient 77% FFSBM in place of 50 and 100% of fractions in soybean products has been evaluated in commercial soybean meal in the control diet had a number of omnivorous fish species. In general, the similar weight gain and protein gain, but more lipid digestibility coefficients obtained for various deposition compared to fish fed the control diet. constituents in soybean products typically have been Another catfish species, Clarius gariepinus, also was rather high, indicating a large percentage of those observed to have similar weight gain and feed constituents can be digested and absorbed by the fish efficiency when FFSBM replaced as much as 44.6% for further metabolism (Table 1). peanut meal in the control diet (Baloguna and Ologhobo, 1989). The digestibility of the protein fraction of soybean products consistently has been reported to be more Another soybean product that has been used than 90% for species such as common carp, channel sparingly in the diet of most fish species is soybean catfish, tilapia and silver perch, with values for some

Table 1: Digestibility Coefficients of Various Soybean Products for Selected Freshwater, Omnivorous Fish Species

Feedstuff International Fish Species Digestibility Coefficient (%) Feed Number Dry Protein Lipid Carbo- Energy Matter hydrate Soybean meal, 5-04-604 Channel catfish1 77 81 solvent-extracted, Blue tilapia2 94 54 with hulls Nile tilapia3 91 57 Hybrid tilapia4 95 90 81 Common carp 925, 706, 957 746 626 756, 807

Soybean meal, 5-04-612 Channel catfish 858, 93-979 739 solvent-extracted, Silver perch10 75 95 78 without hulls

Soybean meal, 5-04-597 Silver perch10 77 92 80 dehulled, full-fat

Soybean, whole Silver perch10 84 96 84 expeller 1 Cruz (1975) 5 Pongmaneerat and Watanabe (1993a) 9 Wilson and Poe (1985) 2 Popma (1982) 6 Degani et al. (1997b) 10 Allan et al. (2000) 3 Hanley (1987) 7 Takeuchi et al. (2002) 4 Degani et al. (1997a) 8 Brown et al. (1985)

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 3 species at or above 95%. The protein digestibility to the considerable expense of fish meals and coefficients compare favorably with those of any concern regarding their limited availability as other high-quality protein feedstuff such as various aquaculture continues to expand, evaluation of fish meals (NRC, 1993). The availability of appropriate substitutes for fish meal has been a individual amino acids in the protein fraction of longstanding research priority (Hardy, 1999). Most soybean products has been determined for only a of the extensive research has been conducted with few fish species such as the tabl carp, channel catfish some of the freshwater, omnivorous species that are and silver perch (Table 2). However, based on data well established in aquaculture. These species obtained from those species, the apparent typically do not exhibit reduced acceptability of availability of all dispensable and indispensable prepared diets containing plant feedstuffs and are amino acids is rather high with the lowest values generally less dependent on fish meal and other averaging 81% for channel catfish and the highest protein feedstuffs of animal origin compared to values averaging between 91 and 95% for common carnivorous species. Therefore, the ability to carp and silver perch, respectively. Thus, in substitute soybean meal for fish meal in diet consideration of the rather high protein digestibility formulations for these species is substantial, as coefficients of soybean products for other summarized in the following studies. omnivorous species, high availability of amino acids to those various species is expected. However, Early studies with common carp indicated reduction amino acid availability data should be obtained for of fish meal from 15 to 5% in low-protein diets individual species so that diets for those species can (25%) by increasing soybean meal from 15 to 35% be formulated more precisely on an available amino caused growth reduction which could not be altered acid basis. by supplementation of additional methionine or lipid (Viola, 1975). However, subsequent experiments Lipid digestibility in soybean meal also is rather (Viola et al., 1981, 1981/1982) demonstrated that high, with values ranging from 74 to 90% for total replacement of fish meal (as much as 25% of channel catfish and common carp, respectively the diet) with soybean meal (as much as 45% of the (Table 1). digestibility in soybean diet) could be achieved by supplementation of lipid products has not been determined, but presumably (up to 10%), methionine (0.4%) and lysine (0.4- would be lower than the other energy-yielding 0.5%) to the soybean meal-based diet. nutrient groups due to the presence of non-starch polysaccharides and indigestible fiber. A Similar results were obtained in another study in carbohydrate digestibility coefficient of 54% was which high-protein (37%) diets were evaluated with reported for blue tilapia (Oreochromis aureus). common carp (Pongmaneerat et al., 1993b). In that Limited digestibility of this fraction primarily is study, a control diet containing 45% brown fish meal responsible for reducing overall dry matter was compared to diets in which the fish meal was digestibility coefficients which have been reported replaced progressively with combinations of to range from 74 to 90% (Table 1). soybean meal, corn meal and/or meal. Reducing fish meal from 45% as in the control diet Energy digestibility from various soybean products to 22% along with 25% soybean meal and 10% corn is high, with values ranging from 57 to 84% gluten meal resulted in similar weight gain, feed (Table 1). Based on these values, the digestible efficiency and protein efficiency ratio (PER) of energy content of solvent-extracted soybean is common carp. Further replacement of fish meal with typically around 3,000 kcal/kg (12,500 kJ/kg). The the other ingredient combinations did impair the digestible energy in FFSBM is higher for most measured responses, although supplementation of species due to its higher lipid content. lysine, methionine and threonine in a diet containing 5% meat meal, 15% corn gluten meal and 40% Ingredient Substitutions soybean meal and no fish meal improved weight gain and feed efficiency to 90% in fish fed the Soybean meal, with its relatively high protein control diet. content and complementary blend of amino acids, traditionally has been evaluated compared to fish Similar results were obtained in a second experiment meal, which is generally considered the most in which an amino acid and methionine mixture was nutritious protein feedstuff for aquatic animals. Due added to diets containing 5% meat meal, 14% corn

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 4 gluten meal and 38% soybean meal. This of fish meal with soybean meal or other ingredients supplementation yielded weight gain, feed efficiency such as cottonseed meal or meat and bone meal and PER responses approximately 90% of those without any impairment in growth and feed achieved by carp fed the control diet with 45% efficiency (Robinson and Li, 1993, 1994, 1998; brown fish meal (Pongmaneerat et al., 1993b). Reigh, 1999). Combining soybean meal with other feedstuffs rich in amino acids, such as squilla Several other experiments conducted with channel (Oratosquilla nepa) meal, also has been reported to catfish in ponds have revealed that diets containing support rapid growth of common carp (Nandeesha et 28 to 32% crude protein primarily from soybean al., 1989). meal provide growth equivalent to diets containing some animal protein, such as fish meal and meat and Several studies conducted with young channel bone meal (Robinson and Li, 1999; Robinson et al., catfish in aquaria have shown that a complete 2000; Li et al., 2000b). These diets typically have replacement of fish meal with soybean not required supplementation of any crystalline meal in diet formulations caused some growth amino acids. However, channel catfish have reduction (Andrews and Page, 1974; Mohsen and responded to amino acid supplementation in certain Lovell, 1990), and supplementation with lysine, practical diets, but protein-bound amino acids are methionine and cystine did not provide an used more efficiently than crystalline amino acids improvement (Andrews and Page, 1974). However, (Zarate and Lovell, 1997). one laboratory study reported that a diet containing soybean meal at up to 50% of diet in combination The blue catfish (Ictalurus furcatus) has been shown with distillers grains allowed the complete to use diets containing high percentages of soybean replacement of fish meal without causing growth meal efficiently, although initial investigation reduction of channel catfish (Webster et al., 1992a). indicated complete replacement of fish meal with soybean meal caused reduced growth of Numerous subsequent experiments, in which (Webster et al., 1992b). In subsequent laboratory channel catfish were grown to market size in earthen studies with juvenile fish, the complete replacement ponds, have demonstrated the complete replacement of menhaden fish meal (15% of the diet) was

Table 2: Apparent Amino Acid Availability Values (%) of Soybean Products for Common Carp1, Channel Catfish2, and Silver Perch3

Ingredient Int’l Species Arg Cys His IIe Leu Lys Met Phe Thr Tyr Val Feed # Soybean meal, 5-04- Common 95.8 88.0 92.0 90.3 92.2 92.6 91.2 93.3 87.1 92.1 89.8 solvent- 604 carp extracted, with hulls

Soybean meal, 5-04- Channel 95.4 83.6 77.6 81.0 90.9 80.4 81.3 77.5 78.7 75.5 solvent- 612 catfish extracted, without hulls Silver 97.8 94.1 96.7 94.9 94.8 96.7 95.7 95.6 95.5 96.2 94.8 perch

Soybean meal, 5-04- Silver 95.4 96.5 94.2 92.0 92.2 94.5 95.7 93.1 94.0 93.6 91.2 dehulled, full- 597 perch fat

Soybean, Silver 97.6 94.0 96.8 96.9 96.4 96.9 98.1 97.3 95.5 96.4 96.5 whole expeller perch

1Yamamoto et al. (1998) 2 Wilson et al. (1981) 3 Allan et al. (2000)

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 5 achieved without adversely affecting weight gain or efficiency and protein efficiency than fish fed the feed efficiency by increasing soybean meal from 42 diet with 30% of its protein from soybean meal. to 65% of the diet (Webster et al., 1995a, 1995b). In However, methionine supplementation in the diet those studies, methionine supplementation in diets with soybean meal allowed tilapia to achieve similar without fish meal did not confer additional weight gain, feed efficiency and protein efficiency improvements in fish responses. Blue catfish appear as those fed the control diet. to have a lower dietary protein requirement compared to channel catfish (Webster et al., 2000). In another series of feeding trials with hybrid tilapia, Viola et al. (1988) evaluated 30% crude protein diets The sharptooth catfish (Clarius gariepinus) also containing 55 to 60% soybean meal and no animal have responded favorably to diets containing feedstuffs along with various supplements such as soybean meal. van Weerd et al. (1999) conducted a oil, methionine, lysine and phosphorus. Viola et al. laboratory experiment in which sharptooth catfish concluded that only phosphorus supplementation of were fed diets containing between 47 to 48% crude the soybean meal-based diet was required to achieve protein, with different amounts of fish meal and weight gain and feed efficiency responses similar to soybean meal. Weight gain and feed efficiency of that of fish fed a control diet containing 35% fish fish fed diets containing 41% soybean meal and 29% meal. fish meal were similar to that of fish fed the control diet containing 18% soybean meal and 58% fish In two separate studies (Wu et al., 1995; Tudor et meal. However, diets containing 69% soybean meal al., 1996), Nile tilapia fed diets containing from 35 and 6% fish meal resulted in reduced weight gain to 56% soybean flour and corn gluten feed, but no and feed efficiency. fish meal, had similar weight gain and feed efficiency as fish fed diets containing as much as 6% Tilapia generally have been shown to respond fish meal. In a more recent study (El-Saidy and favorably to the dietary replacement of fish meal Gaber, 2002), Nile tilapia fed a diet containing 55% with soybean meal. Davis and Stickney (1978) soybean meal supplemented with 1% methionine conducted a 4 x 4 factorial experiment in aquaria and 0.5% lysine significantly had better weight gain with blue tilapia to evaluate four different and feed efficiency than fish fed the control diet combinations of soybean meal and fish meal (each containing 20% menhaden fish meal and 30% constituting 0, 33, 67 or 100% of dietary protein) at soybean meal. Unfortunately, the need for individual each of four dietary protein levels (15, 22, 29 and amino acid supplementation in the soybean meal- 36%). Diets containing all protein combinations, based diet could not be evaluated because those diets except the 36% protein diet with 100% fish meal were supplemented with both methionine and lysine. were supplemented with DL-methionine. Fish fed Protein digestibility of the diet containing 55% diets containing 36% protein experienced the soybean meal was similar to that of the diet with greatest weight gain and feed efficiency. These 20% fish meal and 30% soybean meal. responses were not influenced significantly by any combination of soybean meal to fish meal. However, The tambaqui (Colossoma macropomum), a rapidly at the lower dietary protein levels, a general growing fish native to the Amazon region, has used improvement in growth and feed efficiency was seen a diet containing 59% soybean meal efficiently, with increasing amounts of fish meal in the diet. although growth and feed intake was reduced compared to fish fed a diet containing 32.8% fish In another study, Shiau et al. (1987) fed hybrid meal as the main protein feedstuff (van der Meer et tilapia control diets formulated to contain 24 and al., 1997). 32% crude protein exclusively from fish meal. Experimental diets at each protein level contained Diet Evaluations soybean meal either with or without methionine supplementation (0.2 to 0.26%) to replace 30% of As reviewed in the previous section, a number of the fish meal protein. Fish fed the three diets studies have been conducted to compare the containing 24% crude protein showed no differences nutritional value of soybean meal relative to fish in weight gain, feed efficiency or protein efficiency. meal and protein feedstuffs of animal origin. In In contrast, fish fed the 32% protein diet, with all addition to those studies, several other trials have protein from fish meal, had greater weight gain, feed been completed in China by the American Soybean

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 6 Association (ASA) to evaluate specific diet growth than diets H and K diets containing 5% fish formulations with several different omnivorous fish meal in six of eight trials with Nile tilapia, five of species. These production trials have evaluated diet seven trials with common carp, two of two trials formulations with a variety of fish species using the with crucian carp and in a single trial with bream. ASA’s 80:20 technology in which a high-value species of one size group is fed a prepared diet and The ASA has conducted several other demonstration makes up approximately 80% of total fish weight trials with fry, fingerling and growout diets in a while one or more “service” species constitutes the number of different species spanning several years. other 20% of production. Silver carp has been most Various carp species have been the focus of many of commonly used as a service species due to its these trials. One demonstration trial with common efficient utilization of enhanced natural productivity carp (Cremer and Zhang, 1999a) evaluated an supported by feeding prepared diets to the high- extruded diet (designated 32/6 growout) containing value species. 32% crude protein and 6% lipid from 57% soybean meal, 6% corn gluten meal, 29.4% wheat products, During 1995 and 1996, 14 different feeding trials and various oil, vitamin and supplements. were conducted using the 80:20 technology with This diet allowed carp to grow from an average of crucian carp (Carassius auratus gibelio), pacu 35 grams to 623 grams in a 150-day period with a (Piaractus brachyomum), Nile tilapia and Wuchang (FCR) of 1.47:1 and a 97% carp or bream (Megalobram amblycephala) survival rate. Silver carp production and survival (American Soybean Association, 1996a). In seven also was quite acceptable. different trials with crucian carp, a plant-protein- based diet (designated J) containing 50% soybean Excellent results also have been obtained using meal, 5% cottonseed meal, 5% rapeseed meal and soybean meal-based diets with smaller sizes of 10% corn gluten produced similar or better growth mirror carp. In one such study (Cremer et al., compared to a diet containing 5% fish meal, 40% 2001a), mirror carp were reared from 0.6 to 2 grams soybean meal, and similar amounts of the other using a crumbled diet (designated 41/11 fry) ingredients (designated diet H). The same two diets containing 41% crude protein and 11% lipid from and another containing 5% fish meal and 40% 46.3% soybean meal, 15% corn gluten meal, 14% soybean meal (designated diet K) also were meal, 13% wheat and various oil, vitamin evaluated with pacu in two different trials. Pacu and mineral supplements. Then an extruded diet grew rapidly in the trials and no significant (designated 36/7 fingerling) containing 36% crude differences in growth rate were observed among fish protein and 7% lipid from 46.3% soybean meal, fed the two diets with fish meal and the one without 10% corn gluten meal, 8% anchovy meal, 27% fish meal. wheat products and various oil, vitamin and mineral supplements was fed to the fish for the remainder of In another production trial with Nile tilapia, diet K the 85-day production period. At the end of the trial, containing fish meal provided between 13 and 17% fish averaged 165 grams and their FCR averaged better growth and feed efficiency compared to diet J 1.24:1. In addition, production of silver carp also without fish meal, although tilapia grew rapidly on was achieved using the 80:20 production both diets. However, another trial with fingerling technology. Nile tilapia showed no growth differences in fish fed diets J and H. Three other feeding trials were Similar trials were conducted with crucian carp from conducted with bream to evaluate diets H, J and K. fry to fingerling (Cremer and Zhang, 1999b), and In those trials, bream fed the plant-protein-based diet fingerling to market size (Cremer and Zhang, 1999c; grew as well as those fed the diets containing 5% Cremer et al., 2000a). Fry were fed a 41/11 fish meal. crumbled diet (including 46% soybean meal and 14% anchovy meal) from 0.14 gram to The previously described plant-protein-based diet approximately 10 grams, then converted to the and diets containing 5 to 10% fish meal also were extruded 36/7 diet (including 46% soybean meal and evaluated with several different omnivorous species 8% anchovy meal) until attaining an average of 50 in 23 cage trials during 1995 and 1996 (American grams in 150 days with an average FCR of 1.8:1. Soybean Association 1996b). In these trials, the Similar diets have been used to grow wuchang carp plant-protein-based diet J produced similar or better from 0.2 to 44 grams in 117 days with an FCR of

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 7 1.36:1 (Cremer et al., 2000b). At 50 grams, crucian exhibited excellent production efficiency to market carp were fed the 32/6 diet containing 32% protein size using the 32/6 all-plant-protein extruded diet. In and 6% lipid (including 53% soybean meal and no one such production trial, catfish grew from 126 to fish meal) to a market size of 200 grams with an 570 grams in 139 days with an FCR of 1.61:1 FCR of 1.63:1 in 164 days (Cremer et al., 2000a). A (Cremer et al., 2001c). similar all-plant protein diet allowed groups of crucian carp initially averaging 32, 44 and 64 grams In another trial, catfish grew from 59 to 672 grams to attain market size of 250 grams in 150 to165 days in 156 days with an FCR of 1.44:1 (Cremer et al., with FCR values ranging from 1.5:1 to 1.61:1 2001d). The 32/6 all-plant-protein extruded diet also (Cremer and Zhang, 1999c). provided rapid growth and an average FCR of 1.6 when normal and albino channel catfish were Diets for specific stages of grass carp production cultured in cages (Cremer et al., 2000f). Results of also have been evaluated in China. Grass carp fry these various production trials in China are fed the 41/11 soybean meal-based crumbled diet consistent with the diet evaluations conducted in the until approximately 5 grams and then converted to United States with channel catfish grown to market the extruded 36/7 diet attained 83 grams in 121 days size in earthen ponds. Several of these studies with an FCR of 1.12 (Cremer and Zhang, 1999d). (Robinson and Li, 1993, 1994, 1998, 1999; The 32/6 extruded all-plant-protein diet also Robinson et al., 2000; Reigh, 1999; Li et al., 2000) provided excellent growth of grass carp from have demonstrated the complete replacement of fish fingerling to market size (750 grams) with an meal with soybean meal or other ingredients, such as average FRC of 1.2:1 (Cremer and Zhang, 1999e). cottonseed meal or meat and bone meal without any However, a diet containing 32% protein, 3% lipid impairment in growth and feed efficiency of channel and 8% fiber from 50% soybean meal and 16% soy catfish. The level of soybean meal in those diets hulls provided the most cost-effective production of generally is as high as 41 to 52%. grass carp in several different production trials with FCR values ranging from 1.2:1 to 1.6:1 (Cremer et Soybean Meal Research Efforts al., 2000c, 2001b). Other practical diet formulations for grass carp have typically contained from 24 to Potential negative effects of nitrogen, phosphorus 30% crude protein and routinely included and organic matter releases from aquaculture approximately 50% soybean meal (Ding, 1991). systems to the environment have received considerable attention in recent years (Gatlin and Bigmouth buffalo (Ictiobus sp.) is another species Hardy, 2002). Phosphorus and nitrogen of dietary that has responded favorably to soybean meal-based origin are two primary excretory products of diets and the 80:20 technology. In one aquacultured organisms which are of concern demonstration, buffalo fry were fed the 41/11 because they may contribute to eutrophication of crumbled diet from 0.5 to 10 grams and then aquatic systems. Fish also produce organic wastes converted to the 36/7 extruded diet until attaining a from undigested components of the diet that final average weight of 60 grams in 106 days with contribute to the biochemical oxygen demand of an average FCR of 0.93:1 (Cremer and Zhang, aquaculture systems. More efficient utilization of 1999f). The all-plant-protein 32/6 extruded diet dietary phosphorus, nitrogen (from protein) and supported growth of buffalo from 60 grams to an organic matter will contribute directly to reducing average of 464 grams in 120 days with an average the environmental impact of aquaculture. This FCR of 0.99:1 (Cremer et al., 2000d). increased efficiency of nutrient utilization is particularly important as various sectors of the Channel catfish also have been cultured through aquaculture industry are projected to expand and various phases using soybean meal-based diets and intensify production in the next decade to meet the the 80:20 pond technology. In one trial, catfish fry ever-increasing demand for seafood (Tidwell and were fed the 41/11 diet in crumble form from initial Allan, 2002). stocking to approximately 2 grams then converted to the 36/7 extruded fingerling diet. Fry grew from 1.7 The potential for increased use of soybean meal in grams to an average of 49 grams in 101 days of aquaculture diets is substantial due to its nutritional feeding with an FCR of 0.93:1 (Cremer et al., value and cost-effectiveness compared to other 2000e). Channel catfish fingerlings also have protein feedstuffs. Increasing the availability of

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 8 nutrients from soybean meal could possibly enhance Soybean meal also contains non-starch its aquaculture, while reducing the potential for polysaccharides, such as galactomannan, that are not excretion of enriching nutrients by the cultured digested efficiently by most monogastric animals, organisms. including fish. The use of exogenous enzymes, such as xylanase, α-galactosidase, β-glucanase and endo- Phosphorus in soybean meal is primarily in its β-mannanase, to make this oligosaccharide fraction organic form as phytin phosphorus or phytate, which more digestible has shown positive results in some typically comprises approximately 67% of terrestrial species such as (Ward and Fodge, phosphorus in plant feedstuffs. This form of 1996; Lobo, 1999a). Enhanced digestion of this phosphorus is not readily available to monogastric fraction in soybean meal would not only increase the animals including various fish species (NRC, 1993; digestible energy of this feedstuff, but also limit the Buyukates et al., 2000) because of their lack of amount of organic wastes excreted by the fish. The phytase, the enzyme required to liberate phosphorus physical constraint of applying these heat-labile from phytate. Although diets based on soybean meal enzymes to aquafeeds produced by extrusion generally contain less phosphorus than diets processing will be the same as previously mentioned containing animal feedstuffs, increasing the with phytase supplementation (Lobo, 1999b). availability of phosphorus from soybean products is desirable to restrict the amount of supplemental Another area of research that needs to be addressed phosphorus required in diets and also limit the in greater detail is determining the availability of amount excreted by fish into the environment. amino acids in soybean meal with more omnivorous species. Information currently is available for only a Several studies have shown that addition of fungal few species and has been obtained in a limited phosphorus to soybean meal-based diets can number of experiments. More information effectively increase the availability of phosphorus to concerning amino acid availability of soybean meal various fish species such as common carp (Schafer to various species may allow for more flexibility in et al., 1995), channel catfish (Jackson et al., 1996; using soybean meal as well as assist in refinement of Eya and Lovell, 1997; Li and Robinson, 1997; Yan diet formulations. Increasing this base of et al., 2002) and sharptooth catfish (van Weerd et al., information may result in more precise formulation 1999). However, the instability of phytase to heat of diets on an available amino acid basis so that the normally encountered in feed manufacturing has amino acid requirements of the fish can be met more restricted its use in diet formulations for fish. accurately. Such refinement also may increase the Nevertheless, development of low-temperature efficiency of amino acid utilization by the fish and manufacturing techniques and application of phytase thus limit nitrogen excretion into the environment. after extrusion has provided increased opportunities for its use in the diets of aquatic species. At this time the other primary constraint for supplementing phytase in diets for aquatic species is the cost of the enzyme. Another approach to limit the amount of phytin phosphorus in soybean meal is to develop low phytic acid mutations as has been done for other important agronomic crops, such as corn and barley (Sugiura et al., 1999).

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 9 References Cremer, M.C., Zhang, J., Zhou Enhua, 2000c. Growth performance of grass carp fed a low-fat, high fiber feed formulated with soybean meal and soy hulls as the primary Abel, H.K., Becker, K., Meske, C.H.R., Friedrich, W., 1984. protein and fiber sources. American Soybean Association, Possibilities of using heat-treated full-fat soybeans in carp Beijing, P.R. China. feeding. Aquaculture 42, 97-108. Cremer, M.C., Zhang, J., Zhou Enhua, 2000d. Bigmouth Allan, G.L., Parkinson, S., Booth, M.A., Stone, D.A.J., Buffalo fingerling to market growth performance in ponds in Rowland, S.J., Frances, J., Warner-Smith, R., 2000. Harbin on a soymeal-based feed. American Soybean Replacement of fish meal in diets for Australian silver Association, Beijing, P.R. China. perch, Bidyanus bidyanus: I. Digestibility of alternative Cremer, M.C., Zhang, J., Zhou Enhua, 2000e. Channel catfish ingredients. 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Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 10 Escaffre, A.M., Zambonino Infante, J.L., Cahu, C.L., Mambrini, Reigh, R.C., 1999. Production characteristics of pond-raised M., Bergot, P., Kaushik, S.J., 1997. Nutritional value of soy channel catfish Ictalurus punctatus fed diets with and protein concentrate for larvae of common carp (Cyprinus without animal protein for three growing seasons. J. World carpio) based on growth performance and digestive enzyme Aquaculture Soc. 30, 154-160. activities. Aquaculture 153, 63-80. Robinson, E.H., Li, M.H., 1993. Protein quantity and quality of Eya, J.C., Lovell, R.T., 1997. Net absorption of dietary catfish feeds. Technical Bulletin 189, Mississippi phosphorus from various inorganic sources and effect of Agricultural and Forestry Experiment Station, Mississippi fungal phytase on net absorption of plant phosphorus by State, MS, 10 pp. channel catfish Ictalurus punctatus. J. World Aquaculture Robinson, E.H., Li, M.H., 1994. 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Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 11 Tudor, K.W., Rosati, R.R., O’Rourke, P.D., Wu, Y.V., Sessa, Webster, C.D., Goodgame-Tiu, L.S., Tidwell, J.H., 1995b. Total D., Brown, P., 1996. Technical and economical feasibility of replacement of fish meal by soybean meal, with various on-farm fish feed production using fishmeal analogs. percentages of supplemental L-methionine, in diets for blue 1, 53-65. catfish, Ictalurus furcatus (Lesueur). Aquaculture Research van der Meer, M.B., Faber, R., Zamora, J.E., Verdegem, M.C.J., 26, 299-306. 1997. Effect of feeding level on feed losses and feed Webster, C.D., Tiu, L.G., Morgan, A.M., Gannam, A.L., 2000. utilization of soya and fish meal diets in Colossoma Differences in growth in blue catfish Ictalurus furcatus and macropomum (Cuvier). Aquaculture Research 28, 391-403. channel catfish I. punctatus fed low-protein diets with and van Weerd, J.H., Khalaf, K.H.A., Aartsen, F.J., Tussen, P.A.T., without supplemental methionine and/or lysine. J. World 1999. Balance trials with African catfish Clarius gariepinus Aquaculture Soc. 31, 195-205. fed phytase-treated soybean meal-based diets. Aquaculture Wee, K.L., Shu, S.-W., 1989. The nutritive value of boiled full- Nutrition 5, 135-142. fat soybean in pelleted feed for Nile tilapia. Aquaculture 81, Viola, S., 1975. Experiments on nutrition of carp growing in 303-314. cages part 2. Partial substitution of fish meal. Bamidgeh 27, Wilson, R.P., Poe, W.E., 1985. Apparent digestible protein and 40-48. energy coefficients of common feed ingredients for channel Viola, S., Arieli, J., Rappaport, U., Mokady, S., 1981. catfish. Prog. Fish-Cult. 47, 154-158. Experiments in the nutrition of carp replacement of fishmeal Wilson, R.P., Robinson, E.H., Poe, W.E., 1981. Apparent and by soybean meal. Bamidgeh 33, 35-49. true availability of amino acids from common feed Viola, S., Mokady, S., Rappaport, U., Arieli, Y., 1981/1982. ingredients for channel catfish. J. Nutr. 111, 923-929. Partial and complete replacement of fishmeal by soybean Wu, Y.V., Rosati, R., Sessa, D.J., Brown, P.B., 1995. Utilization meal in feeds for intensive culture of carp. Aquaculture 26, of corn gluten feed by Nile tilapia. Prog. Fish-Cult. 57, 305- 223-236. 309. Viola, S., Mokady, S., Arieli, Y., 1983. Effects of soybean Yamamoto, T., Akimoto, A., Kishi, S., Unuma, T., Akiyama, T., processing methods on the growth of carp (Cyprinus 1998. Apparent and true availabilities of amino acids from carpio). Aquaculture 32, 27-38. several protein sources for fingerling rainbow trout, common Viola, S., Arieli, Y., Zohar, G., 1988. Animal-protein-free feeds carp, and red sea bream. Fisheries Sci. 64, 448-458. for hybrid tilapia (Oreochromis niloticus x O. aureus) in Yan, W., Reigh, R.C., Xu, Z., 2002. Effects of fungal phytase intensive culture. Aquaculture 75, 115-125. on utilization of dietary protein and minerals, and Ward, N.E., Fodge, D., 1996. Soybean-based feeds need dephosphorylation of phytic acid in the alimentary tract of enzymes too. Feed Mgmt. 47, 13-17. channel catfish Ictalurus punctatus fed all-plant-protein diet. Webster, C.D., Tidwell, J.H., Goodgame, L.S., Yancey, D.H., J. World Aquaculture Soc. 33, 10-22. Mackey, L., 1992a. Use of soybean meal and distillers Zarate, D.D., Lovell, R.T., 1997. Free lysine (L-lysine.HCl) is grains with solubles as partial or total replacement of fish utilized for growth less efficiently than protein-bound lysine meal in diets for channel catfish (Ictalurus punctatus). (soybean meal) in practical diets by young channel catfish Aquaculture 106, 301-309. (Ictalurus punctatus). Aquaculture 159, 87-100. Webster, C.D., Yancey, D.H., Tidwell, J.H., 1992b. Effect of partially or totally replacing fish meal with soybean meal on growth of blue catfish (Ictalurus furcatus). Aquaculture 103, 141-152. Webster, C.D., Tidwell, J.H., Tiu, L.S., Yancey, D.H., 1995a. Use of soybean meal as partial or total substitute of fish meal in diets for blue catfish (Ictalurus furcatus). Aquat. Living Resour. 8, 379-384.

Use of Soybean Meal in the Diets of Omnivorous Freshwater Fish -- 12 Managed Aquaculture Program

This technical review paper was created through the Managed Aquaculture Marketing and Research Program (AquaSoy Initiative), funded through the United Soybean Board and American Soybean Association. The AquaSoy Initiative is designed to remove the barriers to soybean meal use in diets fed to aquaculture species. The program has been divided into two components, one focused on awareness, the other on research.

The awareness program initially focuses on Southeast Asia and India, where there are significant opportunities to intensify production within established aquaculture industries with the use of soybean meal-based diets.

The focus of the research component is salmonids, specifically rainbow trout and Atlantic , and commercial , all of which are large industries currently underutilizing soybean meal. The highly integrated and collaborative nature of this initial series of projects should result in expansion of soybean meal into new rapidly growing existing markets in North America, Europe and Asia.

This paper is one of a series of four technical review papers prepared by aquaculture specialists that summarize soy product use and potential in the diets for key aquaculture species groups. The technical reviews address the following species groups: 1) freshwater omnivorous fish; 2) marine fish; 3) marine ; and 4) salmonids. All of these papers can be viewed at www.soymeal.org. United Soybean Board 16640 Chesterfield Grove Road Suite 130 Chesterfield, MO 63005 800/989-USB1 (8721) www.unitedsoybean.org

American Soybean Association Headquarters 12125 Woodcrest Executive Drive, Suite 100 St. Louis, MO 63141-5009 800/688-7692; 314/576-1770 www.soygrowers.com